Pantherophis Guttatus) on Avian Nests

Home , Gray ratsnake, Pantherophis, Pantherophis obsoletus

Herpetological Conservation and Biology 11(1):150–159. Submitted: 9 October 2015; Accepted: 5 April 2016; Published: 30 April 2016.

ECOLOGY AND PREDATION BEHAVIOR OF CORN SNAKES (PANTHEROPHIS GUTTATUS) ON AVIAN NESTS

1,2,3 1 1,2 BRETT A. DEGREGORIO , PATRICK J. WEATHERHEAD , AND JINELLE H. SPERRY

1Department of Natural Resources and Environmental Science, University of Illinois at Urbana, Champaign, 1102 S. Goodwin Drive, Urbana, Illinois 61801, USA 2 U.S. Army Corps of Engineers, ERDC-CERL, 2902 Newmark Drive, Champaign, Illinois 61821, USA 3Corresponding author, e-mail: [email protected]

Abstract.—Relatively little is known about the ecology of free-ranging Corn Snakes (Pantherophis guttatus), although they have been implicated as regionally important avian nest predators. We used nest camera data from 97 snake predation events, 25% of which were attributable to Corn Snakes, to assess how the ecology and behavior of nest predation by Corn Snakes compares to that of sympatric snakes that predate nests. Unlike Ratsnakes (P. alleghaniensis) and Racers (Coluber constrictor), Corn Snakes more frequently preyed on nests located away from forest edges. Nest predation by Corn Snakes, like that by Ratsnakes and Racers, increased over the nesting season. Of the four snake species documented preying on nests at our site, Corn Snakes were the only exclusively nocturnal nest predator, arriving at nests between 2024 and 0220. Corn Snakes were nearly five times more likely to prey on nestlings than eggs, suggesting that they may locate nests visually during the day. On four occasions Corn Snakes arrived at nests shortly after or while other snakes preyed on nestlings, indicating that Corn Snakes may use cues provided by other snakes to locate prey. Unlike other snake species, Corn Snakes never struck at adult birds on the nest and often actually pushed sleeping adults off the nest or pushed under them to access nestlings. Although Corn Snakes do not appear to present nesting birds with unique challenges for avoiding predation, Corn Snakes do present researchers with intriguing questions about their foraging behavior.

Key Words.—activity patterns; behavior; Black Racers; Corn Snakes; edge effects; nest predation; Ratsnakes

INTRODUCTION Avian nest predation risk can be influenced by the location of nests within the landscape. For example, the Growing evidence from video cameras placed at avian influence of forest edges on nest predation risk by snakes nests (Cox et al. 2012a) implicates snakes as major nest has been well documented. Snakes often use forest predators (Weatherhead and Blouin-Demers 2004; edges (e.g., Blouin-Demers and Weatherhead 2001; DeGregorio et al. 2014a). The importance of nest Carfagno and Weatherhead 2006), which leads to predation to breeding birds has therefore led to growing increased nest predation by snakes near edges (Sperry et research on the ecology of nest predation by snakes (e.g., al. 2009; Cox et al. 2012b; DeGregorio et al. 2014b). Weatherhead and Blouin-Demers 2004; Robinson et al. Snakes may also prey more frequently on nests in shrub 2005; Stake et al. 2005; Klug et al. 2010; Visco and habitats than in forests (Thompson and Burhans 2003). Sherry 2015). In North America, Eastern and Texas Similarly, Klug et al. (2010) showed that snakes in Ratsnakes (Pantherophis alleghaniensis and P. grasslands were often found in shrubby patches and that obsoletus) have been a focus of much of that research, as nest predation was highest in these patches. However, both species are major predators of avian nests (e.g., because no study to date has focused on the Corn Snake, Thompson et al. 1999; Stake and Cimprich 2003; Stake it is not known whether this species also exhibits similar et al. 2004, 2005; DeGregorio et al. 2014a). Other snake foraging patterns. species that are regionally significant nest predators, Nest predation risk by snakes can be temporally such as the Corn Snake (P. guttatus: Fig. 1) in the variable. For instance, at some but not all locations, nest southeastern US and the Fox Snake (P. gloydi and P. predation by Eastern and Texas Ratsnakes increases vulpinus) in the Great Lakes region of North America, during the times of the season when they are most active have received less attention despite their importance to (Sperry et al. 2008, 2012; Weatherhead et al. 2010). the birds on whose nests they prey. Determining how Likewise, nest predation by Racers (Coluber constrictor) patterns of predation between species of snakes is increases through the nesting season as Racers become necessary to assess whether different snake species more active (Weatherhead et al. 2010; DeGregorio et al. present nesting birds with unique challenges for reducing 2016). Differences in daily foraging patterns at varying the risk of predation.

FIGURE 1. A Corn Snake (Pantherophis guttatus) leaving a Brown Thrasher (Toxostoma rufum) nest after eating the nestlings at the Savannah River Site, South Carolina, USA, 2011. (Photographed by user-built miniature video camera). latitudes and between species can also be observed. Corn Snakes was greater on edges as would be expected Video evidence shows that Eastern and Texas Ratsnakes if Corn Snakes are edge specialists like Texas and prey on nests during the day at northern latitudes but Eastern Ratsnakes, (2) assess seasonal and daily patterns nocturnally at southern locations (Stake et al. 2005; in nest predation by Corn Snakes, and (3) document the Carter et al. 2007). Nest predation by Racers is strictly behavior of Corn Snakes at avian nests. We studied the diurnal (Stake et al. 2005; Carter et al. 2007; DeGregorio success of snakes at capturing adult birds, frequency et al. 2015) and predation by Corn Snakes at a site in with which they pin nestlings during predation, the Florida was strictly nocturnal (Carter et al. 2007). duration of nest visits, and the frequency with which Finally, video recordings of snake predation provide Corn Snakes visit nests with other snakes. insight into both the behavior of the snakes and implications for the birds on whose nests they prey. MATERIALS AND METHODS Texas Ratsnakes and Great Plains Ratsnakes (P. emoryi) have been documented capturing sleeping adult female Study site and study species.—We studied snakes at birds on the nest (Stake 2001; Reidy et al. 2009), which the Savannah River Site, which encompasses 900 km2 in potentially has demographic implications for bird Aiken and Barnwell counties, South Carolina, USA. populations. Stake et al. (2005) reported that Eastern The site consists of diverse upland and lowland habitats and Texas Ratsnakes often use the coils of their body to and there is no public access. Our study took place at pin nestlings and prevent escape. It is unknown if Corn the Ellenton Bay Set Aside Research area located in the Snakes also employ this sophisticated behavior when east-central portion of the Savannah River Site. The set preying on nestlings. Interestingly, Carter et al. (2007) aside area is a roughly 200-ha area centered around reported that Corn Snakes often arrived at nests as other Ellenton Bay, a 10-ha ephemeral wetland surrounded by snakes preyed on the nest. In two instances, Corn mixed and highly fragmented forests interspersed with Snakes arrived at nests shortly after another Corn Snake open shrubby areas, and dirt roads and power line right- or Eastern Ratsnake had found the nest and in another of-ways. Although the boundaries of the set aside area instance an Eastern Ratsnake arrived at a nest as a Corn encompass a 200-ha area, our study expanded beyond Snake was swallowing nestlings and used its body to these boundaries to the surroundings areas to encompass prevent the Corn Snake from accessing the remaining approximately 900 ha. nestlings. Whether these observations are evidence of The Corn Snake is medium-sized (to 180 cm total social foraging by Corn Snakes is currently unknown. length) constrictor found in many habitat types We used miniature surveillance cameras at bird nests throughout the Southeastern US (Ernst and Ernst 2003). to better understand the foraging behavior of Corn Encounters of most Corn Snakes occur from April to Snakes in relation to other snake species. The objectives June and their daily activity appears to be primarily of our research were to (1) determine if nest predation by nocturnal (Ernst and Ernst 2003). Mating extends from

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March into June and females lay eggs in June and July in know whether this was more than one individual. For mammal burrows and rotting logs and stumps. Although quantification of predator behavior (i.e., timing of visits), reported as a common predator of avian eggs and we extracted behavioral data from each visit. If more nestlings (e.g., Carter et al. 2007), Corn Snakes eat a than one predator species removed contents from the variety of warm-blooded prey, and mammals likely same nest, we considered these independent events. constitute the largest proportion of their diet (Hamilton and Pollack 1956). Nest site characteristics.—After avian nesting had concluded each year (late July to early August), we Nest videography.—To assess the effects of temporal measured a suite of nest site variables that we a priori and nest-site characteristics on predation by Corn hypothesized could influence nest vulnerability to Corn Snakes, we located and monitored nests of a variety of Snakes. These variables included nest height, distance shrub and low-canopy nesting bird species during the to nearest potential snake retreat structure (snag, brush avian nesting seasons of 2011–2013. Because our goals pile, stump, or log), distance to nearest forest edge, were to monitor and film the contents of nests, we distance to nearest overstory tree, diameter of the restricted our nest monitoring to nests < 3 m off the supporting branch, and canopy cover. We measured nest ground. We located nests by intensively searching height to the nearest cm from the ground to the bottom suitable nesting habitat and by noting behavioral cues of each nest using a measuring tape. We also measured provided by nesting birds. We filmed nests using 15 distance to the nearest overstory tree, forest edge, and user-built miniature video systems (Cox et al. 2012a). snake retreat structure with a measuring tape to the We placed cameras 0.5–1 m from nests and camouflaged nearest cm. Overstory trees were defined as trees taller them with vegetation to reduce the likelihood of the than 7 m. We considered forest edge to be the interface cameras attracting predators. Research suggests that between any forested habitat patch and any open habitat nest cameras do not increase the rate of predation for patch or road. If the nearest forest edge was further than filmed nests and in many cases may decrease predation 100 m, we used a GPS unit (Garmin Rino 610, Garmin rates (Richardson et al. 2009). We put cameras only at Ltd., Olathe, Kansas, USA) to measure the distance. We nests that were incubating or brooding to reduce the risk defined a potential snake retreat structure as any of nest abandonment. We checked nests every 48 h to structure large enough for an adult Corn Snake to confirm they were still active and to change the memory completely conceal itself in or under and that would cards in the DVRs. Cameras were powered by deep- prevent an observer from capturing the snake. Thus, a cycle marine batteries, which we changed every 7–10 d. log or a snag had to be substantial enough to conceal and Following predation of a nest, we reviewed the video protect a large snake from capture. We measured the to identify the predator, the behaviors exhibited by the diameter of the branch that most supported each nest predator and the nesting bird, and to document the time using a measuring tape. Canopy cover was visually of the predation event. Because some snakes locate estimated to the nearest 10% immediately above each nests during the day but wait until night to prey on them nest. (Stake et al. 2005; DeGregorio et al. 2015), we also reviewed all of the video starting at sunrise of the day of Statistical analysis.—To assess the influence of these the predation event and watched until sunrise of the nest-site variables on predation by Corn Snakes, we used following day to document any visits to the nest by a multinomial logistic regression model with Proc snakes prior to or following the predation event. We GLIMMIX in SAS 9.2 (SAS Institute, Cary, North recorded details of any interactions between predators at Carolina, USA). The data consisted of each 24-h nests and events in which more than one snake species interval a nest was filmed and the response of each nest visited the same nest. We identified all predators to at the end of the interval. Responses were predation by species (when possible) and recorded the start and end Corn Snake, Eastern Ratsnake, Racer, other predator time of each nest visit by a predator. We determined (mammalian, avian, or arthropod), or survived (our start of a nest predation event by recording when the reference group). We excluded nests for which predator predator was first visible to the camera and determined identity could not be determined as a result of camera the end of the event to be when the predator left the view failure and nests that failed for reasons unrelated to of the camera and did not return for at least 5 min. All predation (e.g., weather). We evaluated support for each nests were filmed until they either fledged or were of the following independent variables: canopy cover, preyed on and then we moved the camera to another nest nest height, distance to nearest edge, distance to nearest to film as many nests as possible each season. snake retreat structure, distance to nearest overstory tree, For analyses of factors influencing predation by Corn diameter of the supporting branch, nesting guild, nest Snakes, we considered multiple visits to a nest from the stage, day of season (Julian date), and maximum daily same predator species as one predation event, even if temperature. they occurred on different days, because we did not

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Because we were unable to film enough nests of TABLE 1. Contents of songbird nests preyed on by Corn Snakes different bird species to analyze separately, we (Pantherophis guttatus), Eastern Ratsnakes (P. alleghaniensis), and Black Racers (Coluber constrictor) at the Savannah River Site, South combined all bird species. However, we did include a Carolina, USA, 2011-2013. variable for nesting guild to look for differences in predator identity at ground nests, open shrub nests (those Nest Stage Corn Snake Ratsnake Black Racer located in shrubs within open habitats such as power line Eggs 4 6 4 right-of-ways or shrublands), closed shrub nests (those Nestlings 16 32 11 located in dense shrubs), and tree nests. Although this Post-Predation or 4 0 2 variable does not account for individual species Fledglings behaviors, it does capture the nesting heterogeneity displayed by the species we monitored. We obtained max daily temperature from a nearby (7 km) weather days: 376), Brown Thrasher (Toxostoma rufum; nests: station and chose this weather variable among many 27, exposure days: 409), and Indigo Bunting (Passerina available because it has been shown to influence nest cyanea; nests: 19, exposure days: 322). We confirmed predation by snakes (Cox et al. 2013). We categorized predator identity for 137 predation events (DeGregorio each nest according to the stage of the contents such that et al. 2014b). These include 10 occasions in which more each nest was either incubating (contained eggs but than one predator preyed on the same nest. Snakes laying had ceased) or had nestlings (contained young collectively were the most frequent nest predators, birds). accounting for 80 predation events. Eastern Ratsnakes To assess differences in the timing of nest predation (hereafter Ratsnake) were the most frequent snake nest by Corn Snakes relative to other snake species, we predator species (38 nest failures; 28% of all nest recorded the time that snakes arrived at each nest for failures), followed by Corn Snakes (20 nest failures; each predation event (not including return visits). To 15%), Black Racers (17 nest failures; 12%), and normalize these data for analyses, we took the difference Coachwhips (Masticophis flagellum: five nest failures; in minutes between snake arrival time and sunset for that 4%). Including return visits and predation events with date (civil twilight times using http://www.sunrise more than one snake at a nest, we collected data for 39 sunset.com). We assessed the effects of species, month, nest visits by Ratsnakes, 24 visits by Corn Snakes, 24 by and a month by species interaction term using a Racers, and 10 by Coachwhips. Because Coachwhips generalized linear model (Proc GLM). We then used accounted for so few nest failures (n = 5), we restricted Tukey’s post-hoc tests to make pair-wise comparisons formal comparisons of Corn Snakes to Ratsnakes and between Corn Snakes and Eastern Ratsnakes and Corn Racers. In addition to the 137 confirmed nest predation Snakes and Racers. Although data were normalized for events, we failed to identify predators at 12 events and analyses, when we discuss raw time data, we present documented 67 successful fledging events. medians and quartiles. We explored differences between the duration of nest Influence of nest characteristics on predation.— predation by different snake species using a Kruskal- Snakes were more likely to prey on nestlings than eggs Wallis test. We have previously reported on the (F8,1819 = 4.13, P < 0.001), although the effect size varied differences in duration between predation by Racers and by snake species. Corn Snakes and Ratsnakes were 4.5– Eastern Ratsnakes and between Eastern Ratsnake 5 times more likely to prey on nestlings than eggs (β = predation during the day and night (DeGregorio et al. ˗1.510; 85% CI: ˗1.600 to ˗1.420, β = ˗1.647; 85% CI: 2015), but present this information again here for ˗1.724 to ˗1.570, respectively; Table 1). Racers were comparative purposes with Corn Snakes. We made pair- also more likely to prey on nestlings than eggs although wise comparisons of predation duration between species the effect size was smaller (β = 0.979; 85% CI: ˗1.078 to (including diurnal vs. nocturnal Eastern Ratsnake ˗0.881). predation) using Wilcoxon Rank Sum tests. All analyses Predation rate by Corn Snakes increased the further were performed with either SAS 9.1 (SAS Institute Inc., that nests were from forest edges (β = 0.009; 85% CI: Cary, North Carolina) or SPSS 22.0 (IBM Corp., 0.008–0.035). This effect was most apparent at large Chicago, Illinois) using an α = 0.05. distances from forest edge. We recorded Corn Snakes preying on nests both in shrublands and deep in forest RESULTS patches. Conversely, Ratsnakes and Racers were more likely to prey on nests located near forest edges We deployed nest cameras at 206 nests of 13 species (Ratsnake: β = -0.005; 85% CI: ˗0.006 to ˗0.004; Racer: of birds. These were primarily the Northern Cardinal β = ˗0.011; 85% CI: ˗0.013 to ˗0.010; Fig. 2). (Cardinalis cardinalis; nests: 85, exposure days: 1,447), Distance to nearest retreat structure also influenced Blue Grosbeak (Passerina caerulea; nests: 25, exposure daily predation rate by snakes overall (F5,1824 = 2.81, P =

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FIGURE 3. Seasonal trends in daily nest predation rate (85% confidence intervals) by Corn Snakes (Pantherophis guttatus), at the Savannah River Site determined via nest videography 2011–2013.

Timing and duration of nest predation.—Different snake species depredated nests at different times of the day (F2,80 = 39.33, P = 0.001). However, month and the month by species interaction term did not affect when snake species preyed on nests (F3,80 = 1.19, P = 0.320 and F8,80 = 1.29, P = 0.260, respectively; Fig. 4). Corn Snakes were the only exclusively nocturnal predator and nests between 2024 and 0220 with a median time preyed on of 2145 (2122–2216: first-third quartiles). Ratsnakes were the only species to prey on nests during both day and night, but most Ratsnake nest visits occurred shortly after sunset (mean = 12 min after sunset, range: 2000 and 2200; median = 2058: 2025–2134). Although Corn Snakes generally depredated nests later at night than Ratsnakes, the difference between the median times of nest predation by the two species was not significant when considering only nocturnal nest visits by Ratsnakes FIGURE 2. Influence of distance from nearest forest edge on daily nest predation rate (85% confidence intervals) by Corn Snakes (P = 0.188). Black Racers were exclusively diurnal and (Pantherophis guttatus), Eastern Ratsnakes (P. alleghaniensis), and visited nests between 0936 and 1734 (median = 1352: Black Racers (Coluber constrictor) at the Savannah River Site, South 1145–1616). Corn Snakes and Ratsnakes each visited Carolina, USA, 2011–2013. nests later in the day than Racers (P = 0.001 and P = 0.004, respectively). 0.015), but differently by species. Predation by Corn The duration of nest visits varied by species, primarily Snakes was not related to distance to retreat structure (β driven by the large difference in duration between Corn = 0.006; 85% CI: 0.003, 0.008) but increased with Snakes and Racers (χ2 = 30.75, df = 3, P < 0.001; Fig. 5). proximity to retreat structures for Ratsnakes (β = ˗0.022; On average, nest visits by Corn Snakes lasted 35.8 min ± 85% CI: ˗0.024, ˗0.019) and decreased with proximity to 8.9 (mean ± SE). Nest visits by Ratsnakes and Racers retreat structures for Racers (β = 0.0334; 85% CI: 0.031– lasted 24.30 min ± 3.09 and 3.82 min ± 1.03, 0.035). Predation rate by snakes was not influenced by respectively. There was no significant difference macrohabitat type (F5,1824 = 2.81, P = 0.150), canopy between the duration of Corn Snake and Ratsnake visits cover (F5,1824 = 1.57, P = 0.167), nest height (F5,1824 = (all Ratsnake visits combined: χ2 = 0.06, df = 2, P = 1.00, P = 0.416), diameter of the supporting branch 0.806). As reported in DeGregorio et al. (2015), (F5,1824 = 1.05, P = 0.385), distance to the nearest tree nocturnal Ratsnake visits lasted three times longer than (F5,1824 = 1.03, P = 0.397), nesting guild (F14,1814 = 1.39, diurnal predations (χ2 = 8.105, df = 2, P = 0.015; mean P = 0.151), or maximum daily temperature (F5,1824 = night = 26.03 ± 3.05 min vs. mean day: 8.00 ± 4.2 min). 1.81, P = 0.108). Although day of year was not significant (F5,1824 = 1.00, P = 0.414), daily predation Predatory behavior.—We observed pinning of rate by Corn Snakes did increase throughout the nesting nestlings in the nest by Ratsnakes only five times (6%) season (Fig. 3). and only once (6%) by a Corn Snake. We did not

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Herpetological Conservation and Biology 11(1):150–159. Submitted: 9 October 2015; Accepted: 5 April 2016; Published: 30 April 2016.

FIGURE 4. Time of day that Corn Snakes (Pantherophis guttatus), Eastern Ratsnakes (P. alleghaniensis), and Black Racers (Coluber constrictor) preyed on songbird nests at the Savannah River Site determined via nest videography 2011–2013. observe Racers using this tactic. Racers frequently occasions, adult birds were either not present (n = 1) or carried prey items away from the nest (36%) to swallow flushed before the snake was within striking distance (n them, presumably to minimize risk of adult nest defense = 4). Ratsnakes visibly struck at adult birds in only three or exposure to other predators. Ratsnakes and Corn of 17 cases when the adult was present, but we never Snakes almost always consumed prey at the nest (96% documented Ratsnakes approaching close enough to and 93% of the time, respectively) and on the occasions adults to make contact with them like Corn Snakes when they did not, it appeared that snakes fell from the routinely did. Conversely, Racers struck at adult birds, nest while manipulating nestlings. but never successfully, in five of six nest predation During our study, snakes were never observed events in which the adult was present. capturing an adult bird. Corn Snakes came within striking distance of adult birds on the nest 11 times. On Inter and intraspecific interactions at nests.—On six of these occasions Corn Snakes used their head to seven occasions we documented multiple snakes visiting push adult birds off the nest or attempted to access nest the same nest and Corn Snakes were involved in four of contents by forcing their way under the bird and into the these events. The first occasion entailed a Corn Snake nest. On most of these occasions, snakes appeared large attempting to gain access to a Brown Thrasher nest as a enough to capture and eat the adult bird (e.g., adult Corn Ratsnake swallowed one of two nestlings. The Ratsnake Snake and Painted Bunting, Passerina ciris) but showed tightly coiled its body over the nest, and prevented the no aggression towards them. During the other Corn Snake from gaining access to the uneaten nestling. five When the Corn Snake retreated, the Ratsnake swallowed the second nestling. The Corn Snake returned to the nest 44 min later and spent 28 min actively tongue flicking and moving about the nest and left without eating an unhatched egg. On another occasion two Corn Snakes arrived at a Blue Grosbeak nest at the same time. Due to heavy rain, we cannot provide further details other than that both snakes were in the nest from 2142–2153 and all of the nestlings were eaten. On two other occasions, we observed Corn Snakes arriving at nests after other snakes had depredated them (3 h 59 min after a Racer and 48 min after a Ratsnake). We recorded three occurrences of other snake species preying on nests following predation by a different snake. In one case a Coachwhip flushed an incubating

female Northern Cardinal off its nest containing three FIGURE 5. Duration of nest visits by Corn Snakes (Pantherophis eggs. The Coachwhip made two trips to the nest and guttatus), Eastern Ratsnakes (P. alleghaniensis), and Black Racers swallowed one egg each time. Six hours and nine (Coluber constrictor) at the Savannah River Site 2011–2013. minutes later a Racer arrived and ate the final egg. In the second example a Ratsnake visited a Northern

Cardinal nest and ate two nestlings 9 h and 40 min after nestling stage than during incubation. Corn Snakes a Racer had visited the nest and eaten the first of the differed from the other species, however, in daily timing three nestlings. The final incident involved two of predation, being exclusively nocturnal nest predators. Ratsnakes visiting the same White-eyed Vireo (Vireo Greater incidence of nest predation during the nestling griseus) nest. On 25 April 2012, we heard the distress period has been interpreted as snakes observing parental calls of adult White-eyed Vireos and discovered a feeding visits to locate nests (Mullin and Cooper 1998). Ratsnake moving away from the nest and being If this interpretation is correct, then snakes that are vigorously attacked by the adult birds. We captured the nocturnal nest predators, such as Corn Snakes and Ratsnake as part of a radio-telemetry study. Our video Ratsnakes, must locate nests during the day when birds indicated that the snake had made contact with the nest are feeding nestlings, but wait until dark to depredate containing four nestlings (5–6 d old) and retreated from these nests. We recently presented indirect evidence for the nest. That night (2025) a different Ratsnake Ratsnakes consistent with this hypothesis: Ratsnakes are depredated the nestlings. most active during the day but prey on nests most at night (Degregorio et al. 2015). We do not know when DISCUSSION Corn Snakes are active, but anecdotally, we rarely encountered Corn Snakes during the day while in the At the Savannah River Site in South Carolina, we field, whereas we encounter Ratsnakes and Racers documented four species of snakes depredating avian regularly. nests. Corn Snakes accounted for 25% of predation by Although Stake et al. (2005) reported Ratsnakes and snakes, confirming a previous report from Florida Eastern King Snakes (Lampropeltis getula) covering the (Carter et al. 2007) that Corn Snakes can be locally top of nests and pinning nestlings with their bodies important nest predators in the southeastern US. Similar during 41% of predation events during the nestling to the report from Florida (Carter et al. 2007), Corn period, we observed this behavior by Ratsnakes only five Snakes at our site were exclusively nocturnal nest times (6%) and only once (6%) by a Corn Snake during predators and more frequently preyed on nestlings than the nestling period. Ratsnakes may employ this eggs. Corn Snakes exhibited different nest depredation technique more frequently during the day when nestlings behavior than the other sympatric snake species in the may be better able to elude capture outside of the nest. region, but not in ways that seem likely to favor different At our site, most nest predation by Ratsnakes and Corn avian nesting strategies to reduce predation risk. Snakes occurred primarily after dark (85 and 100% of Many species of snake preferentially use forest edges, nest predation events) when nestlings forced to fledge a pattern that corresponds with higher rates of nest from the nest would be unlikely to elude capture by predation by snakes (e.g., Sperry et al. 2009; Cox et al. nocturnal snakes. 2012b; DeGregorio et al. 2014b). However, unlike other A seemingly paradoxical aspect of Corn Snake nest snakes at our site, predation risk by Corn Snakes was predation was the absence of any attempt to capture greater away from forest edges. Despite the statistical adult birds on the nest, despite regular opportunities to differences in edge association between Corn Snakes, do so. Adult birds on the nest can be vulnerable to Ratsnakes, and Racers, there was still considerable predation by nocturnal snakes (Reidy et al. 2009), and overlap in habitat. Corn Snakes were documented Ratsnakes and Racers both made unsuccessful strikes at preying on nests in both shrub habitats and forest adults they encountered as they approached nests. By interior, so the breadth of habitat use appears similar contrast, Corn Snakes often reached nests without among the snakes that prey on avian nests within our disturbing the adult, but then either pushed the adult off study area. Similarly, our results indicated that with the nest or pushed under the adult to access the nestlings. minor differences, Corn Snakes did not prey on nests Limited gape size cannot explain why Corn Snakes did associated with different microhabitat features from not attempt to capture adults of at least smaller prey those preyed on by other sympatric snake species (e.g., species, given that those adults were smaller than some Ratsnake predation associated with retreat sites). These of the nestlings of larger species that Corn Snakes results suggest that where Corn Snakes are abundant, the consumed over the course of the study (e.g., adult Indigo risk of nest predation by snakes does not substantially or Painted Buntings compared to Brown Thrasher alter where in the habitat of the bird that the risk occurs. nestlings). It is possible that the commotion associated Thus, the opportunity for birds to alter predation risk with subduing an adult bird could cause premature from snakes by changing where they nest does not fledging of the nestlings, resulting in the Corn Snake change with the addition of Corn Snakes to the snake getting a lower return from a nest than when it focuses fauna. exclusively on capturing nestlings. Our observations Similar to Ratsnakes and Racers, nest predation by suggest that Corn Snakes are unlikely to be responsible Corn Snakes increased throughout the bird nesting for the death of many adult birds on the nest, unlike what season and occurred much more frequently during the has been reported for Ratsnakes and Great Plains

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Ratsnakes in some locations (Stake 2001; Reidy et al. Jason Norman and the Hammond Hills Animal Hospital 2009). for transmitter surgeries. Animals were collected under We documented several instances of interactions SC Department of Natural Resources permits # G-11-03 between two snakes at a nest or of a snake arriving at and 23-2012A. Animal procedures conformed to nests following predation by another snake. Corn permits approved by the Universities of Illinois (IACUC Snakes were common participants, but not the only #11054) and Georgia (AUP #A2011 04-007-Y2-A0). species involved in these interactions. Carter et al. (2007) previously documented three instances of Corn LITERATURE CITED Snakes interacting with other snakes at nests. This type of interaction appears to occur more often than would be Blouin‐Demers, G., and P.J. Weatherhead. 2001. An expected if the participating snakes were finding nests experimental test of the link between foraging, habitat independently. We filmed nests for an average of 16 (± selection and thermoregulation in Black Ratsnakes 7 SD) d and only 58% were preyed on by snakes, so for Elaphe obsoleta obsoleta. Journal of Animal two snakes to arrive at the same nest at or close to the Ecology 70:1006–1013. same time would be a rare event if it occurred by chance. Carfagno, G.L.F, and P.J. Weatherhead. 2006. The most likely explanation for this behavior is that Intraspecific and interspecific variation in use of snakes (Corn Snakes in particular) sometimes actively forest-edge habitat by snakes. Canadian Journal of follow other snakes. Often snakes do not consume the Zoology 84:1440–1452. entire contents of nests, so by following another snake Carter, G.M., M.L. Legare, D.R. Breininger, and D.M. the follower may occasionally benefit from scavenging Oddy. 2007. Nocturnal nest predation: a potential what is left by the other snake. Scavenging could obstacle to recovery of a Florida Scrub‐Jay population. include capturing nestlings that eluded capture by other Journal of Field Ornithology 78:390–394. snakes by leaping out of the nest. We have documented Clark, R.W. 2004. Timber Rattlesnakes (Crotalus snakes capturing nestlings outside the nest and we have horridus) use chemical cues to select ambush sites. evidence of nestlings eluding capture and surviving until Journal of Chemical Ecology 30:607–617. the following day by jumping from the nest, so it is Costanzo, J.P. 1989. Conspecific scent trailing by garter unclear how vulnerable nestlings are to snakes after snakes (Thamnophis sirtalis) during autumn: Further leaving the nest. Snakes have been documented evidence for use of pheromones in den location. following scent trails of other snakes to hibernation sites Journal of Chemical Ecology 15:2531–2538. (e.g., Costanzo 1989), but we are unaware of any Cox, W.A., M.S. Pruett, T.J. Benson, S.J. Chiavacci, and previous evidence of scent trailing being used as part of F.R. Thompson III. 2012a. Development of camera a foraging strategy, although Timber Rattlesnakes technology for monitoring nests. Studies in Avian (Crotalus horridus) may use cues from conspecifics to Biology 43:185–198. select successful ambush sites (Clark 2004). Cox, W.A., F.R. Thompson III, and J. Faaborg. 2012b. Our study has raised a number of questions about Landscape forest cover and edge effects on songbird Corn Snake behavior, particularly regarding how they nest predation vary by nest predator. Landscape find avian nests and the potential role of social foraging. Ecology 27:659–669. Further studies are required to address these questions to Cox, W.A., F.R. Thompson III, and J.L. Reidy. 2013. better understand Corn Snake foraging ecology and The effects of temperature on nest predation by behavior. It may also be important to study these mammals, birds, and snakes. Auk 130:784–790. questions across the range of a species if their foraging DeGregorio, B.A., S.J. Chiavacci, P.J. Weatherhead, behavior varies regionally as it does for the Eastern J.D. Willson, T.J. Benson, and J.H. Sperry. 2014a. Ratsnake. Snake predation on North American bird nests: culprits, patterns and future directions. Journal of Acknowledgments.—Funding was provided by the Avian Biology 45:325–333. Construction Engineering Research Laboratory of the DeGregorio, B.A., J.H. Sperry, and P.J. Weatherhead. Engineer Research Development Center. We thank Tim 2015. Wait until dark? Daily activity patterns and nest Hayden for arranging funding. Special thanks to the predation by snakes. Ethology 121:1–10. Savannah River Ecology Lab for hosting us, particularly DeGregorio, B.A., P.J. Weatherhead, and J.H. Sperry. Tracey Tuberville and Brian Metts. We thank all of our 2014b. Power lines, roads, and avian nest survival: technicians including Eric Nordberg, Mary Mack Gray, effects on predator identity and predation intensity. Ashley Smith, Patrick Barnhart, Patrick Roberts, Phil Ecology and Evolution 4:1589–1600. Vogrinc, Emily Williams, Mae Cowgill, Sara Wendt, DeGregorio, B.A., P.J. Weatherhead, M.P. Ward, and Clay Noss, and Andrew Cronin. We thank Scott J.H. Sperry. 2016. Do seasonal patterns of Ratsnake Chiavacci for assistance with nest cameras and Kirk (Pantherophis obsoletus) and Black Racer (Coluber Stodola for his statistical assistance. We also thank Dr.

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constrictor) activity predict avian nest predation? variation in nest predation risk for birds. Journal of Ecology and Evolution 2016:1–10. Avian Biology 39:379–383. Ernst, C.H., and E.M. Ernst. 2003. Snakes of the United Stake, M.M. 2001. Predation by a Great Plains Ratsnake States and Canada. Smithsonian Books, Washington, on an adult female Golden-cheeked Warbler. Wilson D.C., and London, USA and UK. Bulletin 113:460–461. Hamilton, W.J., Jr., and J.A. Pollack. 1956. The food of Stake, M.M., and D.A. Cimprich. 2003. Using video to some colubrid snakes from Fort Benning, Georgia. monitor predation at Black-capped Vireo nests. Ecology 37:519–526. Condor 105:348–357. Klug, P.E., S.L. Jackrel, and K.A. With. 2010. Linking Stake, M.M., J. Faaborg, and F.R. Thompson III. 2004. snake habitat use to nest predation risk in grassland Video identification of predators at Golden-cheeked birds: the dangers of shrub cover. Oecologia 162:803– Warbler nests. Journal of Field Ornithology 75:337– 813. 344. Mullin, S.J., and R.J. Cooper. 1998. The foraging Stake, M.M., F.R. Thompson III, J. Faaborg, and D.E. ecology of the Gray Ratsnake (Elaphe obsoleta Burhans. 2005. Patterns of snake predation at songbird spiloides) - visual stimuli facilitate location of arboreal nests in Missouri and Texas. Journal of Herpetology prey. American Midland Naturalist 140:397–401. 39:215–222. Reidy, J.L., M.M. Stake, and F.R. Thompson III. 2009. Thompson III, F.R., and D.E. Burhans. 2003. Predation Nocturnal predation of females on nests: an important of songbird nests differs by predator source of mortality for Golden-cheeked Warblers? and between field and forest habitats. Journal of Wildlife Wilson Journal of Ornithology 121:416–421. Management 67:408–416. Richardson, T., T. Gardali, and S.H. Jenkins. 2009. Thompson III, F.R., W. Dijak, and D.E. Burhans. 1999. Review and meta‐analysis of camera effects on avian Video identification of predators at songbird nests in nest success. Journal of Wildlife Management 73:287– old fields. Auk 1999:259–264. 293. Visco, D.M., and T.W. Sherry. 2015. Increased Robinson, W.D., R., Ghislain, and T.R. Robinson. 2005. abundance, but reduced nest predation in the Chestnut- Videography of Panama bird nests shows snakes are backed Antbird in Costa Rican rainforest fragments: principal predators. Ornitologia Neotropical 16:187– surprising impacts of a pervasive snake species. 195. Biological Conservation 188:22–31. Sperry, J. H., D.G. Barron, and P.J. Weatherhead. 2012: Weatherhead, P.J., and G. Blouin‐Demers. 2004. Snake behavior and seasonal variation in nest survival Understanding avian nest predation: why of northern cardinals Cardinalis cardinalis. Journal of ornithologists should study snakes. Journal of Avian Avian Biology 43:496–502. Biology 35:185–190. Sperry, J.H., D.A. Cimprich, R.G. Peak, and P.J. Weatherhead, P.J., G.L.F Carfagno, J.H. Sperry, J.D. Weatherhead. 2009. Is nest predation on two Brawn, and S.K. Robinson. 2010. Linking snake endangered bird species higher in habitats preferred by behavior to nest predation in a Midwestern bird snakes? Ecoscience 16:111–118. community. Ecological Applications 20:234–241. Sperry, J. H., R.G. Peak, D.A. Cimprich, and P.J. Weatherhead. 2008. Snake activity affects seasonal

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BRETT DEGREGORIO recently received his Ph.D. from the University of Illinois. His dissertation research focused on snake-bird interactions and the potential influence of climate change. He currently works as a Wildlife Biologist for the US Army Corps of Engineers and focuses on endangered species research on Department of Defense installations. (Photographed by Jacob Hill).

PATRICK J. WEATHERHEAD is a Professor at the University of Illinois, Champaign, Illinois, USA. He received his B.Sc. in Biology from Carleton University, Ottawa, Ontario (1974), and an M.Sc. and Ph.D. in Biology from Queen’s University, Kingston, Ontario (in 1976 and 1978, respectively). His research focuses primarily on the behavior and ecology of snakes and birds, with a particular interest in snake-bird interactions. (Photographed by Kit Muma).

JINELLE H. SPERRY is an Adjunct Assistant Professor at the University of Illinois and a research scientist at the US Army’s Engineer and Research Development Center in Champaign, Illinois. Her research has focused on the core theme of community ecology and the effects of human-caused disturbances to multi-species interactions. (Photographed by Christopher Taylor).

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